Introduction

Evolution of extended breath-hold
endurance enables the exploitation of the aquatic niche by numerous
mammalian lineages and
is accomplished by elevated body oxygen
stores and morphological and physiological adaptations that promote
their economical
use. High muscle myoglobin concentrations in
particular are mechanistically linked with an extended dive capacity
phenotype,
yet little is known regarding the molecular
and biochemical underpinnings of this key specialization. We modeled the
evolutionary
history of this respiratory pigment over 200
million years of mammalian evolution to elucidate the development of
maximal
diving capacity during the major mammalian
land-to-water transitions.

Evolutionary reconstruction of myoglobin net surface charge in terrestrial and aquatic mammals.
The figure reveals a molecular signature of elevated myoglobin net
surface charge in all lineages of living elite mammalian
divers with an extended aquatic history
(upper silhouettes). This signature is used here to infer the diving
capacity of extinct
species representing stages during
mammalian land-to-water transitions (†).

Methods

We first determined the relationship
between maximum myoglobin concentration and its sequence-derived net
surface charge across
living mammalian taxa. By using ancestral
sequence reconstruction we then traced myoglobin net surface charge
across a 130-species
phylogeny to infer ancestral myoglobin muscle
concentrations. Last, we estimated maximum dive time in extinct
transitional
species on the basis of the relationship of
this variable with muscle myoglobin concentration and body mass in
extant diving
mammals.

Results

We reveal an adaptive molecular
signature of elevated myoglobin net surface charge in all lineages of
mammalian divers with
an extended aquatic history—from 16-g water
shrews to 80,000-kg whales—that correlates with exponential increases in
muscle
myoglobin concentrations. Integration of this
data with body mass predicts 82% of maximal dive-time variation across
all degrees
of diving ability in living mammals.

Discussion

We suggest that the convergent
evolution of high myoglobin net surface charge in mammalian divers
increases intermolecular
electrostatic repulsion, permitting higher
muscle oxygen storage capacities without potentially deleterious
self-association
of the protein. Together with fossil
body-mass estimates, our evolutionary reconstruction permits detailed
assessments of
maximal submergence times and potential
foraging ecologies of early transitional ancestors of cetaceans,
pinnipeds, and sea
cows.Our findings support
amphibious ancestries for echidnas, talpid moles, hyraxes, and
elephants, thereby not only establishing
the earliest land-to-water transition among
placental mammals but also providing a new perspective on the evolution
of myoglobin,
arguably the best-known protein.